Differential mechanical response of mesenchymal stem cells and fibroblasts to tumor-secreted soluble factors

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  McGrail, Daniel J ^a   Ghosh, Deepraj ^a   Quach, Nhat D ^b   Dawson, Michelle R ^a,b  

^a Georgia Institute of Technology   (United States)

^b GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN CDC42; RAC1 PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; NEUROPEPTIDE; RAC PROTEIN; RAC1 PROTEIN, MOUSE; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHOA PROTEIN, MOUSE;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; CELL ADHESION; CELL ELONGATION; CONTROLLED STUDY; CULTURE MEDIUM; CYTOSKELETON; FIBROBLAST; FLOW KINETICS; MESENCHYMAL STEM CELL; MOLECULAR MECHANICS; MORPHOLOGY; MOUSE; NONHUMAN; PHENOMENOLOGY; PHENOTYPIC VARIATION; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; ANIMAL; BIOMECHANICS; CELL MOTION; CELL STRAIN 3T3; CYTOLOGY; EXPERIMENTAL NEOPLASM; FEMALE; FOCAL ADHESION; GENE EXPRESSION; GENETICS; PHYSIOLOGY; SECRETION; SOLUBILITY; TUMOR CELL LINE;

ANIMALS; BIOMECHANICS; CDC42 GTP-BINDING PROTEIN; CELL LINE, TUMOR; CELL MOVEMENT; CULTURE MEDIA, CONDITIONED; CULTURE MEDIA, SERUM-FREE; CYTOSKELETON; FEMALE; FIBROBLASTS; FOCAL ADHESIONS; GENE EXPRESSION; MAMMARY NEOPLASMS, EXPERIMENTAL; MESENCHYMAL STEM CELLS; MICE; NEUROPEPTIDES; RAC GTP-BINDING PROTEINS; RHEOLOGY; RHO GTP-BINDING PROTEINS; SOLUBILITY; SWISS 3T3 CELLS;

EID: 84858422884     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0033248     Document Type: Article

References (60)

1. Balkwill F, Mantovani A, (2001) Inflammation and cancer: back to Virchow? Lancet 357: 539-545.
2. Hanahan D, Weinberg RA, (2011) Hallmarks of cancer: the next generation. Cell 144: 646-674.
3. Covas DT, Panepucci RA, Fontes AM, Silva WA, Orellana MD, et al. (2008) Multipotent mesenchymal stromal cells obtained from diverse human tissues share functional properties and gene-expression profile with CD146+ perivascular cells and fibroblasts. Exp Hematol 36: 642-654.
4. Haniffa MA, Wang X-N, Holtick U, Rae M, Isaacs JD, et al. (2007) Adult Human Fibroblasts Are Potent Immunoregulatory Cells and Functionally Equivalent to Mesenchymal Stem Cells. The Journal of Immunology 179: 1595-1604.
5. Stagg J, (2008) Mesenchymal stem cells in cancer. Stem Cell Rev 4: 119-124.
6. Song S, Ewald AJ, Stallcup W, Werb Z, Bergers G, (2005) PDGFRbeta+ perivascular progenitor cells in tumours regulate pericyte differentiation and vascular survival. Nat Cell Biol 7: 870-879.
7. Karnoub AE, Dash AB, Vo AP, Sullivan A, Brooks MW, et al. (2007) Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature 449: 557-563.
8. Orimo A, Gupta PB, Sgroi DC, Arenzana-Seisdedos F, Delaunay T, et al. (2005) Stromal Fibroblasts Present in Invasive Human Breast Carcinomas Promote Tumor Growth and Angiogenesis through Elevated SDF-1/CXCL12 Secretion. Cell 121: 335-348.
9. Micke P, Tman A, (2004) Tumour-stroma interaction: cancer-associated fibroblasts as novel targets in anti-cancer therapy? Lung Cancer 45, (Supplement 2): S163-S175.
10. Hall B, Andreeff M, Marini F, (2007) The Participation of Mesenchymal Stem Cells in Tumor Stroma Formation and Their Application as Targeted-Gene Delivery Vehicles. In: Kauser K, Zeiher A-M, editors. Bone Marrow-Derived Progenitors Springer Berlin Heidelberg pp. 263-283.
11. Kucerova L, Altanerova V, Matuskova M, Tyciakova S, Altaner C, (2007) Adipose Tissue-Derived Human Mesenchymal Stem Cells Mediated Prodrug Cancer Gene Therapy. Cancer Research 67: 6304-6313.
12. Rønnov-Jessen L, Petersen OW, Koteliansky VE, Bissell MJ, (1995) The origin of the myofibroblasts in breast cancer. Recapitulation of tumor environment in culture unravels diversity and implicates converted fibroblasts and recruited smooth muscle cells. The Journal of Clinical Investigation 95: 859-873.
13. Studeny M, Marini FC, Champlin RE, Zompetta C, Fidler IJ, et al. (2002) Bone marrow-derived mesenchymal stem cells as vehicles for interferon-beta delivery into tumors. Cancer Res 62: 3603-3608.
14. Hung SC, Deng WP, Yang WK, Liu RS, Lee CC, et al. (2005) Mesenchymal stem cell targeting of microscopic tumors and tumor stroma development monitored by noninvasive in vivo positron emission tomography imaging. Clin Cancer Res 11: 7749-7756.
15. Komarova S, Kawakami Y, Stoff-Khalili MA, Curiel DT, Pereboeva L, (2006) Mesenchymal progenitor cells as cellular vehicles for delivery of oncolytic adenoviruses. Mol Cancer Ther 5: 755-766.
16. Nakamura K, Ito Y, Kawano Y, Kurozumi K, Kobune M, et al. (2004) Antitumor effect of genetically engineered mesenchymal stem cells in a rat glioma model. Gene Ther 11: 1155-1164.
17. Khakoo AY, Pati S, Anderson SA, Reid W, Elshal MF, et al. (2006) Human mesenchymal stem cells exert potent antitumorigenic effects in a model of Kaposi's sarcoma. J Exp Med 203: 1235-1247.
18. Rombouts WJC, Ploemacher RE, (2003) Primary murine MSC show highly efficient homing to the bone marrow but lose homing ability following culture. Leukemia 17: 160-170.
19. Dwyer RM, Potter-Beirne SM, Harrington KA, Lowery AJ, Hennessy E, et al. (2007) Monocyte chemotactic protein-1 secreted by primary breast tumors stimulates migration of mesenchymal stem cells. Clin Cancer Res 13: 5020-5027.
20. Kumar S, Nagy TR, Ponnazhagan S, (2010) Therapeutic potential of genetically modified adult stem cells for osteopenia. Gene Ther 17: 105-116.
21. Rosova I, Dao M, Capoccia B, Link D, Nolta JA, (2008) Hypoxic preconditioning results in increased motility and improved therapeutic potential of human mesenchymal stem cells. Stem cells 26: 2173-2182.
22. Ohnishi S, Yasuda T, Kitamura S, Nagaya N, (2007) Effect of Hypoxia on Gene Expression of Bone Marrow-Derived Mesenchymal Stem Cells and Mononuclear Cells. Stem Cells 25: 1166-1177.
23. Ponte AL, Marais E, Gallay N, Langonné A, Delorme B, et al. (2007) The In Vitro Migration Capacity of Human Bone Marrow Mesenchymal Stem Cells: Comparison of Chemokine and Growth Factor Chemotactic Activities. Stem cells 25: 1737-1745.
24. Ozaki Y, Nishimura M, Sekiya K, Suehiro F, Kanawa M, et al. (2007) Comprehensive Analysis of Chemotactic Factors for Bone Marrow Mesenchymal Stem Cells. Stem Cells and Development 16: 119-130.
25. Kole TP, Tseng Y, Huang L, Katz JL, Wirtz D, (2004) Rho kinase regulates the intracellular micromechanical response of adherent cells to rho activation. Mol Biol Cell 15: 3475-3484.
26. Wirtz D, (2009) Particle-Tracking Microrheology of Living Cells: Principles and Applications. Annual Review of Biophysics 38: 301-326.
27. Stossel TP, Condeelis J, Cooley L, Hartwig JH, Noegel A, et al. (2001) Filamins as integrators of cell mechanics and signalling. Nat Rev Mol Cell Biol 2: 138-145.
28. McBeath R, Pirone DM, Nelson CM, Bhadriraju K, Chen CS, (2004) Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Developmental Cell 6: 483-495.
29. Treiser MD, Yang EH, Gordonov S, Cohen DM, Androulakis IP, et al. (2010) Cytoskeleton-based forecasting of stem cell lineage fates. Proceedings of the National Academy of Sciences 107: 610-615.
30. Kilian KA, Bugarija B, Lahn BT, Mrksich M, (2010) Geometric cues for directing the differentiation of mesenchymal stem cells. Proceedings of the National Academy of Sciences 107: 4872-4877.
31. Engler A, Sen S, Sweeney H, Discher D, (2006) Matrix Elasticity Directs Stem Cell Lineage Specification. Cell 126: 677-689.
32. McBeath R, Pirone DM, Nelson CM, Bhadriraju K, Chen CS, (2004) Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev Cell 6: 483-495.
33. Peister A, Mellad JA, Larson BL, Hall BM, Gibson LF, et al. (2004) Adult stem cells from bone marrow (MSCs) isolated from different strains of inbred mice vary in surface epitopes, rates of proliferation, and differentiation potential. Blood 103: 1662-1668.
34. Tropel P, Noël D, Platet N, Legrand P, Benabid A-L, et al. (2004) Isolation and characterisation of mesenchymal stem cells from adult mouse bone marrow. Experimental cell research 295: 395-406.
35. Menon LG, Picinich S, Koneru R, Gao H, Lin SY, et al. (2007) Differential Gene Expression Associated with Migration of Mesenchymal Stem Cells to Conditioned Medium from Tumor Cells or Bone Marrow Cells. Stem Cells 25: 520-528.
36. Lin S-Y, Yang J, Everett AD, Clevenger CV, Koneru M, et al. (2008) The isolation of novel mesenchymal stromal cell chemotactic factors from the conditioned medium of tumor cells. Experimental Cell Research 314: 3107-3117.
37. Klopp AH, Spaeth EL, Dembinski JL, Woodward WA, Munshi A, et al. (2007) Tumor irradiation increases the recruitment of circulating mesenchymal stem cells into the tumor microenvironment. Cancer Res 67: 11687-11695.
38. Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, et al. (2004) Twist, a Master Regulator of Morphogenesis, Plays an Essential Role in Tumor Metastasis. Cell 117: 927-939.
39. Tao K, Fang M, Alroy J, Sahagian GG, (2008) Imagable 4T1 model for the study of late stage breast cancer. BMC Cancer 8: 228.
40. Pigati L, Yaddanapudi SCS, Iyengar R, Kim D-J, Hearn SA, et al. (2010) Selective Release of MicroRNA Species from Normal and Malignant Mammary Epithelial Cells. PloS one 5: e13515.
41. Coussens LM, Werb Z, (2002) Inflammation and cancer. Nature 420: 860-867.
42. Kole TP, Tseng Y, Jiang I, Katz JL, Wirtz D, (2005) Intracellular mechanics of migrating fibroblasts. Mol Biol Cell 16: 328-338.
43. Ponte AL, Marais E, Gallay N, Langonne A, Delorme B, et al. (2007) The in vitro migration capacity of human bone marrow mesenchymal stem cells: comparison of chemokine and growth factor chemotactic activities. Stem Cells 25: 1737-1745.
44. Kim S, Takahashi H, Lin WW, Descargues P, Grivennikov S, et al. (2009) Carcinoma-produced factors activate myeloid cells through TLR2 to stimulate metastasis. Nature 457: 102-106.
45. Wels J, Kaplan RN, Rafii S, Lyden D, (2008) Migratory neighbors and distant invaders: tumor-associated niche cells. Genes Dev 22: 559-574.
46. Daniels BR, Hale CM, Khatau SB, Kusuma S, Dobrowsky TM, et al. (2010) Differences in the Microrheology of Human Embryonic Stem Cells and Human Induced Pluripotent Stem Cells. Biophysical Journal 99: 3563-3570.
47. Maesaki R, Ihara K, Shimizu T, Kuroda S, Kaibuchi K, et al. (1999) The Structural Basis of Rho Effector Recognition Revealed by the Crystal Structure of Human RhoA Complexed with the Effector Domain of PKN/PRK1. Molecular Cell 4: 793-803.
48. Jaganathan BG, Ruester B, Dressel L, Stein S, Grez M, et al. (2007) Rho inhibition induces migration of mesenchymal stromal cells. Stem Cells (Dayton, Ohio) 25: 1966-1974.
49. Tseng Y, (2002) Microheterogeneity Controls the Rate of Gelation of Actin Filament Networks. Journal of Biological Chemistry 277: 18143-18150.
50. Truskey GA, Yuan F, Katz DF, (2009) Transport Phenomena in Biological Systems Upper Saddle River, New Jersey Pearson Educatoin.
51. Ishizaki T, Morishima Y, Okamoto M, Furuyashiki T, Kato T, et al. (2001) Coordination of microtubules and the actin cytoskeleton by the Rho effector mDia1. Nat Cell Biol 3: 8-14.
52. Kozma R, Ahmed S, Best A, Lim L, (1995) The Ras-related protein Cdc42Hs and bradykinin promote formation of peripheral actin microspikes and filopodia in Swiss 3T3 fibroblasts. Molecular and Cellular Biology 15: 1942-1952.
53. Govind S, Kozma R, Clinton M, Lim L, Ahmed S, (2001) Cdc42Hs Facilitates Cytoskeletal Reorganization and Neurite Outgrowth by Localizing the 58-kD Insulin Receptor Substrate to Filamentous Actin. The Journal of Cell Biology 152: 579-594.
54. Chamberlain G, Fox J, Ashton B, Middleton J, (2007) Concise Review: Mesenchymal Stem Cells: Their Phenotype, Differentiation Capacity, Immunological Features, and Potential for Homing. Stem cells 25: 2739-2749.
55. Pajerowski JD, Dahl KN, Zhong FL, Sammak PJ, Discher DE, (2007) Physical plasticity of the nucleus in stem cell differentiation. Proceedings of the National Academy of Sciences 104: 15619-15624.
56. Lee JSH, Chang MI, Tseng Y, Wirtz D, (2005) Cdc42 Mediates Nucleus Movement and MTOC Polarization in Swiss 3T3 Fibroblasts under Mechanical Shear Stress. Molecular Biology of the Cell 16: 871-880.
57. Weir C, Morelkopp M, Gill A, Tinworth K, Ladd L, et al. (2008) Mesenchymal Stem Cells: Isolation, Characterisation and In Vivo Fluorescent Dye Tracking. Heart, Lung and Circulation 17: 395-403.
58. Tseng Y, Kole TP, Wirtz D, (2002) Micromechanical mapping of live cells by multiple-particle-tracking microrheology. Biophys J 83: 3162-3176.
59. Mason TG, (2000) Estimating the viscoelastic moduli of complex fluids using the generalized Stokes-Einstein equation. Rheologica Acta 39: 371-378.
60. Reyes CD, Garcia AJ, (2003) A centrifugation cell adhesion assay for high-throughput screening of biomaterial surfaces. J Biomed Mater Res A 67: 328-333.